Skip to main content

Advertisement

SpringerLink
Log in

Bacterial metabolism of environmental arsenic—mechanisms and biotechnological applications

  • Mini-Review
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Arsenic causes threats for environmental and human health in numerous places around the world mainly due to its carcinogenic potential at low doses. Removing arsenic from contaminated sites is hampered by the occurrence of several oxidation states with different physicochemical properties. The actual state of arsenic strongly depends on its environment whereby microorganisms play important roles in its geochemical cycle. Due to its toxicity, nearly all organisms possess metabolic mechanisms to resist its hazardous effects, mainly by active extrusion, but also by extracellular precipitation, chelation, and intracellular sequestration. Some microbes are even able to actively use various arsenic compounds in their metabolism, either as an electron donor or as a terminal electron acceptor for anaerobic respiration. Some microorganisms can also methylate inorganic arsenic, probably as a resistance mechanism, or demethylate organic arsenicals. Bioavailability of arsenic in water and sediments is strongly influenced by such microbial activities. Therefore, understanding microbial reactions to arsenic is of importance for the development of technologies for improved bioremediation of arsenic-contaminated waters and environments. This review gives an overview of the current knowledge on bacterial interactions with arsenic and on biotechnologies for its detoxification and removal.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Achal V, Pan XL, Fu QL, Zhang DY (2012) Biomineralization based remediation of As(III) contaminated soil by Sporosarcina ginsengisoli. J Hazard Mater 201:178–184

    Article  CAS  Google Scholar 

  • Achour AR, Bauda P, Billard P (2007) Diversity of arsenite transporter genes from arsenic-resistant soil bacteria. Res Microbiol 158:128–137

    Article  CAS  Google Scholar 

  • Achour-Rokbani A, Cordi A, Poupin P, Bauda P, Billard P (2010) Characterization of the ars gene cluster from extremely arsenic-resistant Microbacterium sp strain A33. Appl Environ Microbiol 76:948–955

    Google Scholar 

  • Afkar E, Lisak J, Saltikov C, Basu P, Oremland RS, Stolz JF (2003) The respiratory arsenate reductase from Bacillus selenitireducens strain MLS10. FEMS Microbiol Lett 226:107–112

    Article  CAS  Google Scholar 

  • Ahmann D, Roberts AL, Krumholz LR, Morel FMM (1994) Microbe grows by reducing arsenic. Nature 371(6500):750–750

    Article  CAS  Google Scholar 

  • Ajees AA, Marapakala K, Packianathan C, Sankaran B, Rosen BP (2012) Structure of an As(III) S-adenosylmethionine methyltransferase: insights into the mechanism of arsenic biotransformation. Biochemistry 51:5476–5485

    Article  CAS  Google Scholar 

  • Al M, Evans LJ, Gould WD, Duncan WFA, Glasauer S (2011) The long term operation of a biologically based treatment system that removes As, S and Zn from industrial (smelter operation) landfill seepage. Appl Geochem 26:1886–1896

    Article  CAS  Google Scholar 

  • Anderson GL, Williams J, Hille R (1992) The purification and characterization of arsenite oxidase from Alcaligenes faecalis, a molybdenum-containing hydroxylase. J Biol Chem 267:23674–23682

    CAS  Google Scholar 

  • Arsène-Ploetze F, Koechler S, Marchal M, Coppee JY, Chandler M, Bonnefoy V, Brochier-Armanet C, Barakat M, Barbe V, Battaglia-Brunet F, Bruneel O, Bryan CG, Cleiss-Arnold J, Cruveiller S, Erhardt M, Heinrich-Salmeron A, Hommais F, Joulian C, Krin E, Lieutaud A, Lievremont D, Michel C, Muller D, Ortet P, Proux C, Siguier P, Roche D, Rouy Z, Salvignol G, Slyemi D, Talla E, Weiss S, Weissenbach J, Medigue C, Bertin PN (2010) Structure, Function, and Evolution of the Thiomonas spp. Genome. PLoS Genet 6. doi:10.1371/journal.pgen.1000859

  • Basturea GN, Harris TK, Deutscher MP (2012) Growth of a bacterium that apparently uses arsenic instead of phosphorus is a consequence of massive ribosome breakdown. J Biol Chem 287:28816–28819

    Article  CAS  Google Scholar 

  • Benner SA (2011) Comment on "A bacterium that can grow by using arsenic instead of phosphorus". Science 332(6034). doi:10.1126/science.1201304

  • Bentley R, Chasteen TG (2002) Microbial methylation of metalloids: arsenic, antimony, and bismuth. Microbiol Mol Biol Rev 66:250–271

    Article  CAS  Google Scholar 

  • Bertin PN, Medigue C, Normand P (2008) Advances in environmental genomics: towards an integrated view of micro-organisms and ecosystems. Microbiol-SGM 154:347–359

    Article  CAS  Google Scholar 

  • Bertin PN, Heinrich-Salmeron A, Pelletier E, Goulhen-Chollet F, Arsene-Ploetze F, Gallien S, Lauga B, Casiot C, Calteau A, Vallenet D, Bonnefoy V, Bruneel O, Chane-Woon-Ming B, Cleiss-Arnold J, Duran R, Elbaz-Poulichet F, Fonknechten N, Giloteaux L, Halter D, Koechler S, Marchal M, Mornico D, Schaeffer C, Smith AAT, Van Dorsselaer A, Weissenbach J, Medigue C, Le Paslier D (2011) Metabolic diversity among main microorganisms inside an arsenic-rich ecosystem revealed by meta- and proteo-genomics. ISME J 5:1735–1747

    Article  CAS  Google Scholar 

  • Bertin PN, Geist L, Halter D, Koechler S, Marchal M, Arsene-Ploetze F (2012) Microbial arsenic response and metabolism in the genomics era. In: Santini JM, Ward SA (eds) Arsenic in the environment. CRC Press, Boca Raton, pp 99–114

    Google Scholar 

  • Beveridge TJ, Makin SA, Kadurugamuwa JL, Li ZS (1997) Interactions between biofilms and the environment. FEMS Microbiol Rev 20:291–303

    Article  CAS  Google Scholar 

  • Branco R, Chung AP, Morais PV (2008) Sequencing and expression of two arsenic resistance operons with different functions in the highly arsenic-resistant strain Ochrobactrum tritici SCII24T. BMC Microbiol 8:95. doi:10.1186/1471-2180-8-95

  • Branco R, Francisco R, Chung AP, Morais PV (2009) Identification of an aox system that requires cytochrome c in the highly arsenic-resistant bacterium Ochrobactrum tritici SCII24. Appl Environ Microbiol 75:5141–5147

    Google Scholar 

  • Bryan CG, Marchal M, Battaglia-Brunet F, Kugler V, Lemaitre-Guillier C, Lievremont D, Bertin PN, Arsene-Ploetze F (2009) Carbon and arsenic metabolism in Thiomonas strains: differences revealed diverse adaptation processes. BMC Microbiol 9. doi:10.1186/1471-2180-9-127

  • Carapito C, Muller D, Tarlin E, Koechler S, Danchin A, Van Dorsselaer A, Leize-Wagner E, Bertin PN, Lett MC (2006) Identification of genes and proteins involved in the pleiotropic response to arsenic stress in Caenibacter arsenoxydans, a metalloresistant beta-proteobacterium with an unsequenced genome. Biochimie 88:595–606

    Article  CAS  Google Scholar 

  • Carlin A, Shi WP, Dey S, Rosen BP (1995) The ars operon of Escherichia coli confers arsenical and antimonial resistance. J Bacteriol 177:981–986

    CAS  Google Scholar 

  • Castillo R, Saier MH Jr (2010) Functional promiscuity of homologues of the bacterial ArsA ATPases. Int J Microbiol. doi:10.1155/2010/187373

    Google Scholar 

  • Challenger F (1945) Biological methylation. Chem Rev 36:315–361

    Article  CAS  Google Scholar 

  • Chang WC, Hsu GS, Chiang SM, Su MC (2006) Heavy metal removal from aqueous solution by wasted biomass from a combined AS-biofilm process. Bioresour Technol 97:1503–1508

    Article  CAS  Google Scholar 

  • Chauhan NS, Ranjan R, Purohit HJ, Kalia VC, Sharma R (2009) Identification of genes conferring arsenic resistance to Escherichia coli from an effluent treatment plant sludge metagenomic library. FEMS Microbiol Ecol 67:130–139

    Article  CAS  Google Scholar 

  • Chen CM, Misra TK, Silver S, Rosen BP (1986) Nucleotide-sequence of the structural genes for an anion pump—the plasmid-encoded arsenical resistance operon. J Biol Chem 261:5030–5038

    Google Scholar 

  • Chen J, Zhu YG, Rosen BP (2012) A novel biosensor selective for organoarsenicals. Appl Environ Microbiol 78:7145–7147

    Article  CAS  Google Scholar 

  • Cheng HF, Hu YN, Luo J, Xu B, Zhao JF (2009) Geochemical processes controlling fate and transport of arsenic in acid mine drainage (AMD) and natural systems. J Hazard Mater 165:13–26

    Article  CAS  Google Scholar 

  • Cleiss-Arnold J, Koechler S, Proux C, Fardeau ML, Dillies MA, Coppee JY, Arsene-Ploetze F, Bertin PN (2010) Temporal transcriptomic response during arsenic stress in Herminiimonas arsenicoxydans. BMC Genomics 11. doi:10.1186/1471-2164-11-709

  • Cullen WR, Bentley R (2005) The toxicity of trimethylarsine: an urban myth. J Environ Monitor 7:11–15

    Article  CAS  Google Scholar 

  • Cullen WR, Reimer KJ (1989) Arsenic speciation in the environment. Chem Rev 89:713–764

    Article  CAS  Google Scholar 

  • Dani SU (2010) Arsenic for the fool: an exponential connection. Sci Total Environ 408:1842–1846

    Article  CAS  Google Scholar 

  • de Mora K, Joshi N, Balint BL, Ward FB, Elfick A, French CE (2011) A pH-based biosensor for detection of arsenic in drinking water. Anal Bioanal Chem 400:1031–1039

    Article  CAS  Google Scholar 

  • Delmont TO, Malandain C, Prestat E, Larose C, Monier JM, Simonet P, Vogel TM (2011) Metagenomic mining for microbiologists. ISME J 5:1837–1843

    Article  CAS  Google Scholar 

  • Denef VJ, Kalnejais LH, Mueller RS, Wilmes P, Baker BJ, Thomas BC, VerBerkmoes NC, Hettich RL, Banfield JF (2010a) Proteogenomic basis for ecological divergence of closely related bacteria in natural acidophilic microbial communities. Proc Natl Acad Sci USA 107:2383–2390

    Article  CAS  Google Scholar 

  • Denef VJ, Mueller RS, Banfield JF (2010b) AMD biofilms: using model communities to study microbial evolution and ecological complexity in nature. ISME J 4:599–610

    Article  Google Scholar 

  • Dey S, Rosen BP (1995) Dual-mode of energy coupling by the oxyanion-translocating ArsB protein. J Bacteriol 177:385–389

    CAS  Google Scholar 

  • Diesel E, Schreiber M, van der Meer JR (2009) Development of bacteria-based bioassays for arsenic detection in natural waters. Anal Bioanal Chem 394:687–693

    Article  CAS  Google Scholar 

  • Duquesne K, Lieutaud A, Ratouchniak J, Muller D, Lett MC, Bonnefoy V (2008) Arsenite oxidation by a chemoautotrophic moderately acidophilic Thiomonas sp.: from the strain isolation to the gene study. Environ Microbiol 10:228–237

    CAS  Google Scholar 

  • Dzombak DA, Morel FMM (1990) Surface complexation modeling: hydrous ferric oxide. Wiley, New York

    Google Scholar 

  • Egal M, Casiot C, Morin G, Elbaz-Poulichet F, Cordier MA, Bruneel O (2010) An updated insight into the natural attenuation of As concentrations in Reigous Creek (southern France). Appl Geochem 25:1949–1957

    Article  CAS  Google Scholar 

  • Ellis PJ, Conrads T, Hille R, Kuhn P (2001) Crystal structure of the 100 kDa arsenite oxidase from Alcaligenes faecalis in two crystal forms at 1.64 angstrom and 2.03 angstrom. Structure 9:125–132

    Article  CAS  Google Scholar 

  • Erb TJ, Kiefer P, Hattendorf B, Gunther D, Vorholt JA (2012) GFAJ–1 is an arsenate-resistant, phosphate-dependent organism. Science 337(6093):467–470

    Article  CAS  Google Scholar 

  • Fekry MI, Tipton PA, Gates KS (2011) Kinetic consequences of replacing the internucleotide phosphorus atoms in DNA with arsenic. ACS Chem Biol 6:127–130

    Article  CAS  Google Scholar 

  • Fendorf S, Michael HA, van Geen A (2010) Spatial and temporal variations of groundwater arsenic in south and southeast Asia. Science 328(5982):1123–1127

    Article  CAS  Google Scholar 

  • Ferrer M, Martinez-Abarca F, Golyshin PN (2005) Mining genomes and ‘metagenomes’ for novel catalysts. Curr Opin Biotechnol 16:588–593

    Article  CAS  Google Scholar 

  • Gilmour MW, Thomson NR, Sanders M, Parkhill J, Taylor DE (2004) The complete nucleotide sequence of the resistance plasmid R478: defining the backbone components of incompatibility group H conjugative plasmids through comparative genomics. Plasmid 52:182–202

    Article  CAS  Google Scholar 

  • Gresser MJ (1981) ADP-arsenate—formation by sub-mitochondrial particles under phosphorylating conditions. J Biol Chem 256:5981–5983

    CAS  Google Scholar 

  • Hahn-Tomer S (2011) It introduces itself ARSOlux (R)—biosensor based on a bioreporter bacteria for the detection of arsenic in drinking water. Grundwasser 16:133–134

    Google Scholar 

  • Harms H, Rime J, Leupin O, Hug SJ, van der Meer JR (2005) Effect of groundwater composition on arsenic detection by bacterial biosensors. Microchim Acta 151:217–222

    Article  CAS  Google Scholar 

  • Harrison JJ, Rabiei M, Turner RJ, Badry EA, Sproule KM, Ceri H (2006) Metal resistance in Candida biofilms. FEMS Microbiol Ecol 55:479–491

    Article  CAS  Google Scholar 

  • Hayakawa T, Kobayashi Y, Cui X, Hirano S (2005) A new metabolic pathway of arsenite: arsenic–glutathione complexes are substrates for human arsenic methyltransferase Cyt19. Arch Toxicol 79:193–191

    Article  CAS  Google Scholar 

  • Heinrich-Salmeron A, Cordi A, Brochier-Armanet C, Halter D, Pagnout C, Abbaszadeh-Fard E, Montaut D, Seby F, Bertin PN, Bauda P, Arsene-Ploetze F (2011) Unsuspected diversity of arsenite-oxidizing bacteria as revealed by widespread distribution of the aoxB gene in prokaryotes. Appl Environ Microbiol 77:4685–4692

    Article  CAS  Google Scholar 

  • Hoeft SE, Kulp TR, Stolz JF, Hollibaugh JT, Oremland RS (2004) Dissimilatory arsenate reduction with sulfide as electron donor: experiments with Mono Lake water and isolation of strain MLMS-1, a chemoautotrophic arsenate respirer. Appl Env Microbiol 70:2741–2747

    Article  CAS  Google Scholar 

  • Holmes DE, O’Neil RA, Chavan MA, N'Guessan LA, Vrionis HA, Perpetua LA, Larrahondo MJ, DiDonato R, Liu A, Lovley DR (2009) Transcriptome of Geobacter uraniireducens growing in uranium-contaminated subsurface sediments. ISME J 3:216–230

    Article  CAS  Google Scholar 

  • Hu Q, Li L, Wang YJ, Zhao WJ, Qi HY, Zhuang GQ (2010) Construction of WCB-11: a novel phiYFP arsenic-resistant whole-cell biosensor. J Environ Sci-China 22:1469–1474

    Article  CAS  Google Scholar 

  • Huang YY, Li H, Rensing C, Zhao K, Johnstone L, Wang GJ (2012) Genome sequence of the facultative anaerobic arsenite-oxidizing and nitrate-reducing bacterium Acidovorax sp strain NO1. J Bacteriol 194:1635–1636

    Article  CAS  Google Scholar 

  • Hughes MF (2002) Arsenic toxicity and potential mechanisms of action. Toxicol Lett 133:1–16

    Article  CAS  Google Scholar 

  • Ivanina AV, Shuvaeva OV (2009) Use of a bacterial biosensor system for determining arsenic in natural waters. J Anal Chem 64:310–315

    Article  CAS  Google Scholar 

  • Ji GY, Silver S (1992) Reduction of arsenate to arsenite by the ArsC protein of the arsenic resistance operon of Staphylococcus aureus plasmid pI258. Proc Natl Acad Sci USA 89:9474–9478

    Article  CAS  Google Scholar 

  • Ji GY, Garber EAE, Armes LG, Chen CM, Fuchs JA, Silver S (1994) Arsenate reductase of Staphylococcus aureus plasmid pI258. Biochemistry-US 33:7294–7299

    Article  CAS  Google Scholar 

  • Kang YS, Bothner B, Rensing C, McDermott TR (2012a) Involvement of RpoN in regulating bacterial arsenite oxidation. Appl Environ Microbiol 78:5638–5645

    Article  CAS  Google Scholar 

  • Kang YS, Heinemann J, Bothner B, Rensing C, McDermott TR (2012b) Integrated co-regulation of bacterial arsenic and phosphorus metabolisms. Environ Microbiol 14:3097–3109

    Article  CAS  Google Scholar 

  • Kashyap DR, Botero LM, Franck WL, Hassett DJ, McDermott TR (2006a) Complex regulation of arsenite oxidation in Agrobacterium tumefaciens. J Bacteriol 188:1081–1088

    Article  CAS  Google Scholar 

  • Kashyap DR, Botero LM, Lehr C, Hassett DJ, McDermott TR (2006b) A Na+:H+ antiporter and a molybdate transporter are essential for arsenite oxidation in Agrobacterium tumefaciens. J Bacteriol 188:1577–1584

    Article  CAS  Google Scholar 

  • Kim MJ, Nriagu J, Haack S (2000) Carbonate ions and arsenic dissolution by groundwater. Environ Sci Technol 34:3094–3100

    Article  CAS  Google Scholar 

  • Kim HA, Lee KY, Lee BT, Kim SO, Kim KW (2012) Comparative study of simultaneous removal of As, Cu, and Pb using different combinations of electrokinetics with bioleaching by Acidithiobacillus ferrooxidans. Water Res 46:5591–5599

    Article  CAS  Google Scholar 

  • Kloppers A, Larmuth K, Deane S, Rawlings DE (2008) Leptospirilli from different continents have acquired related arsenic-resistance transposons. Hydrometallurgy 94:170–174

    Article  CAS  Google Scholar 

  • Koechler S, Cleiss-Arnold J, Proux C, Sismeiro O, Dillies MA, Goulhen-Chollet F, Hommais F, Lievremont D, Arsene-Ploetze F, Coppee JY, Bertin PN (2010) Multiple controls affect arsenite oxidase gene expression in Herminiimonas arsenicoxydans. BMC Microbiol 10. doi:10.1186/1471-2180-10-53

  • Kostal J, Yang R, Wu CH, Mulchandani A, Chen W (2004) Enhanced arsenic accumulation in engineered bacterial cells expressing ArsR. Appl Environ Microbiol 70:4582–4587

    Article  CAS  Google Scholar 

  • Kotze AA, Tuffin IM, Deane SM, Rawlings DE (2006) Cloning and characterization of the chromosomal arsenic resistance genes from Acidithiobacillus caldus and enhanced arsenic resistance on conjugal transfer of ars genes located on transposon TnAtcArs. Microbiol-SGM 152:3551–3560

    Article  CAS  Google Scholar 

  • Krafft T, Macy JM (1998) Purification and characterization of the respiratory arsenate reductase of Chrysiogenes arsenatis. Eur J Biochem 255:647–653

    Article  CAS  Google Scholar 

  • Kulp TR, Hoeft SE, Asao M, Madigan MT, Hollibaugh JT, Fisher JC, Stolz JF, Culbertson CW, Miller LG, Oremland RS (2008) Arsenic(III) fuels anoxygenic photosynthesis in hot spring biofilms from Mono Lake, California. Science 321(5891):967–970

    Article  CAS  Google Scholar 

  • Laverman AM, Blum JS, Schaefer JK, Phillips EJP, Lovley DR, Oremland RS (1995) Growth of strain SES-3 with arsenate and other diverse electron-acceptors. Appl Environ Microbiol 61:3556–3561

    CAS  Google Scholar 

  • Lebrun E, Brugna M, Baymann F, Muller D, Lievremont D, Lett MC, Nitschke W (2003) Arsenite oxidase, an ancient bioenergetic enzyme. Mol Biol Evol 20:686–693

    Article  CAS  Google Scholar 

  • Lee KY, Yoon IH, Lee BT, Kim SO, Kim KW (2009) A novel combination of anaerobic bioleaching and electrokinetics for arsenic removal from mine tailing soil. Environ Sci Technol 43:9354–9360

    Article  CAS  Google Scholar 

  • Lehr CR, Polishchuk E, Radoja U, Cullen WR (2003) Demethylation of methylarsenic species by Mycobacterium neoaurum. Appl Organomet Chem 17:831–834

    Article  CAS  Google Scholar 

  • Lett MC, Muller D, Lievremont D, Silver S, Santini J (2012) Unified nomenclature for genes involved in prokaryotic aerobic arsenite oxidation. J Bacteriol 194:207–208

    Article  CAS  Google Scholar 

  • Li XY, Hu Y, Gong J, Lin YB, Johnstone L, Rensing C, Wang GJ (2012) Genome sequence of the highly efficient arsenite-oxidizing bacterium Achromobacter arsenitoxydans SY8. J Bacteriol 194:1243–1244

    Article  CAS  Google Scholar 

  • Lievremont D, Bertin PN, Lett MC (2009) Arsenic in contaminated waters: biogeochemical cycle, microbial metabolism and biotreatment processes. Biochimie 91:1229–1237

    Article  CAS  Google Scholar 

  • Lin YF, Yang JB, Rosen BP (2007) ArsD: an As(III) metallochaperone for the ArsAB As(III)-translocating ATPase. J Bioenerg Biomembr 39:453–458

    Article  CAS  Google Scholar 

  • Liu ZJ, Boles E, Rosen BP (2004) Arsenic trioxide uptake by hexose permeases in Saccharomyces cerevisiae. J Biol Chem 279:17312–17318

    Article  CAS  Google Scholar 

  • Liu ZJ, Sanchez MA, Jiang X, Boles E, Landfear SM, Rosen BP (2006) Mammalian glucose permease GLUT1 facilitates transport of arsenic trioxide and methylarsonous acid. Biochem Biophys Res Commun 351:424–430

    Article  CAS  Google Scholar 

  • Liu S, Zhang F, Chen J, Sun GX (2011) Arsenic removal from contaminated soil via biovolatilization by genetically engineered bacteria under laboratory conditions. J Environ Sci-China 23:1544–1550

    Article  CAS  Google Scholar 

  • Liu GH, Liu MY, Kim EH, Maaty WS, Bothner B, Lei BF, Rensing C, Wang GJ, McDermott TR (2012) A periplasmic arsenite-binding protein involved in regulating arsenite oxidation. Environ Microbiol 14:1624–1634

    Article  CAS  Google Scholar 

  • Lovley DR, Coates JD (1997) Bioremediation of metal contamination. Curr Opin Biotechnol 8:285–289

    Article  CAS  Google Scholar 

  • Ma YF, Wu JF, Wang SY, Jang CY, Zhang Y, Qi SW, Liu L, Zhao GP, Liu SJ (2007) Nucleotide sequence of plasmid pCNB1 from Comamonas strain CNB-1 reveals novel genetic organization and evolution for 4-chloronitrobenzene degradation. Appl Environ Microbiol 73:4477–4483

    Article  CAS  Google Scholar 

  • Macy JM, Rech S, Auling G, Dorsch M, Stackebrandt E, Sly LI (1993) Thauera selenatis gen nov, sp nov, a member of the beta-subclass of proteobacteria with a novel type of anaerobic respiration. Int J Syst Bacteriol 43:135–142

    Article  CAS  Google Scholar 

  • Macy JM, Nunan K, Hagen KD, Dixon DR, Harbour PJ, Cahill M, Sly LI (1996) Chrysiogenes arsenatis gen nov, sp nov; a new arsenate-respiring bacterium isolated from gold mine wastewater. Int J Syst Bacteriol 46:1153–1157

    Article  CAS  Google Scholar 

  • Macy JM, Santini JM, Pauling BV, O’Neill AH, Sly LI (2000) Two new arsenate/sulfate-reducing bacteria: mechanisms of arsenate reduction. Arch Microbiol 173:49–57

    Article  CAS  Google Scholar 

  • Maki T, Takeda N, Hasegawa H, Ueda K (2006) Isolation of monomethylarsonic acid-mineralizing bacteria from arsenic contaminated soils of Ohkunoshima Island. Appl Organomet Chem 20:538–544

    Article  CAS  Google Scholar 

  • Malasarn D, Keeffe JR, Newman DK (2008) Characterization of the arsenate respiratory reductase from Shewanella sp strain ANA-3. J Bacteriol 190:135–142

    Article  CAS  Google Scholar 

  • Marchal M, Briandet R, Halter D, Koechler S, Dubow MS, Lett MC, Bertin PN (2011) Subinhibitory arsenite concentrations lead to population dispersal in Thiomonas sp. PLoS One 6. doi:10.1371/journal.pone.0023181

  • Mcbride BC, Wolfe RS (1971) Biosynthesis of dimethylarsine by Methanobacterium. Biochemistry-US 10:4312–4317

    Article  CAS  Google Scholar 

  • Meng YL, Liu ZJ, Rosen BP (2004) As(III) and Sb(III) uptake by G1pF and efflux by ArsB in Escherichia coli. J Biol Chem 279:18334–18341

    Article  CAS  Google Scholar 

  • Michel C, Jean M, Coulon S, Dictor MC, Delorme F, Morin D, Garrido F (2007) Biofilms of As(III)-oxidising bacteria: formation and activity studies for bioremediation process development. Appl Microbiol Biotechnol 77:457–467

    Article  CAS  Google Scholar 

  • Michel C, Garrido F, Roche E, Belval SC, Dictor MC (2011) Role of exopolymeric substances (EPS) in the stability of the biofilm of Thiomonas arsenivorans grown on a porous mineral support. J Microbiol Biotechnol 21:183–186

    Article  CAS  Google Scholar 

  • Mukhopadhyay R, Rosen BP, Pung LT, Silver S (2002) Microbial arsenic: from geocycles to genes and enzymes. FEMS Microbiol Rev 26:311–325

    Article  CAS  Google Scholar 

  • Muller D, Lievremont D, Simeonova DD, Hubert JC, Lett MC (2003) Arsenite oxidase aox genes from a metal-resistant beta-proteobacterium. J Bacteriol 185:135–141

    Article  CAS  Google Scholar 

  • Muller D, Medigue C, Koechler S, Barbe V, Barakat M, Talla E, Bonnefoy V, Krin E, Arsene-Ploetze F, Carapito C, Chandler M, Cournoyer B, Cruveiller S, Dossat C, Duval S, Heymann M, Leize E, Lieutaud A, Lievremont D, Makita Y, Mangenot S, Nitschke W, Ortet P, Perdrial N, Schoepp B, Siguier P, Simeonova DD, Rouy Z, Segurens B, Turlin E, Vallenet D, Van Dorsselaer A, Weiss S, Weissenbach J, Lett MC, Danchin A, Bertin PN (2007) A tale of two oxidation states: Bacterial colonization of arsenic-rich environments. PLoS Genet 3. doi:10.1371/journal.pgen.0030053

  • Murphy JN, Saltikov CW (2009) The ArsR repressor mediates arsenite-dependent regulation of arsenate respiration and detoxification operons of Shewanella sp strain ANA-3. J Bacteriol 191:6722–6731

    Article  CAS  Google Scholar 

  • Murphy JN, Durbin KJ, Saltikov CW (2009) Functional Roles of arcA, etrA, cyclic AMP (cAMP)-cAMP receptor protein, and cya in the arsenate respiration pathway in Shewanella sp strain ANA-3. J Bacteriol 191:1035–1043

    Article  CAS  Google Scholar 

  • Neculita CM, Zagury GJ, Bussiere B (2007) Passive treatment of acid mine drainage in bioreactors using sulfate-reducing bacteria: Critical review and research needs. J Environ Qual 36:1–16

    Article  CAS  Google Scholar 

  • Neubauer O (1947) Arsenical cancer - a review. Br J Cancer 1:192–251

    Article  CAS  Google Scholar 

  • Newman DK, Beveridge TJ, Morel FMM (1997a) Precipitation of arsenic trisulfide by Desulfotomaculum auripigmentum. Appl Environ Microbiol 63:2022–2028

    CAS  Google Scholar 

  • Newman DK, Kennedy EK, Coates JD, Ahmann D, Ellis DJ, Lovley DR, Morel FMM (1997b) Dissimilatory arsenate and sulfate reduction in Desulfotomaculum auripigmentum sp. nov. Arch Microbiol 168:380–388

    Article  CAS  Google Scholar 

  • Nicolis I, Curis E, Deschamps P, Benazeth S (2009) Arsenite medicinal use, metabolism, pharmacokinetics and monitoring in human hair. Biochimie 91:1260–1267

    Article  CAS  Google Scholar 

  • Niggemyer A, Spring S, Stackebrandt E, Rosenzweig RF (2001) Isolation and characterization of a novel As(V)-reducing bacterium: implications for arsenic mobilization and the genus Desulfitobacterium. Appl Environ Microbiol 67:5568–5580

    Article  CAS  Google Scholar 

  • Nordstrom DK (2002) Public health—worldwide occurrences of arsenic in ground water. Science 296(5576):2143–2145

    Article  CAS  Google Scholar 

  • O’day PA, Vlassopoulos D, Root R, Rivera N (2004) The influence of sulfur and iron on dissolved arsenic concentrations in the shallow subsurface under changing redox conditions. Proc Natl Acad Sci USA 101:13703–13708

    Article  Google Scholar 

  • Ordonez E, Letek M, Valbuena N, Gil JA, Mateos LM (2005) Analysis of genes involved in arsenic resistance in Corynebacterium glutamicum ATCC 13032. Appl Environ Microbiol 71:6206–6215

  • Oremland RS, Stolz JF (2003) The ecology of arsenic. Science 300(5621):939–944

    Article  CAS  Google Scholar 

  • Oremland RS, Stolz JF (2005) Arsenic, microbes and contaminated aquifers. Trends Microbiol 13:45–49

    Article  CAS  Google Scholar 

  • Oremland RS, Hoeft SE, Santini JA, Bano N, Hollibaugh RA, Hollibaugh JT (2002) Anaerobic oxidation of arsenite in Mono Lake water and by facultative, arsenite-oxidizing chemoautotroph, strain MLHE-1. Appl Environ Microbiol 68:4795–4802

    Article  CAS  Google Scholar 

  • Oremland RS, Saltikov CW, Wolfe-Simon F, Stolz JF (2009) Arsenic in the evolution of earth and extraterrestrial ecosystems. Geomicrobiol J 26:522–536

    Article  CAS  Google Scholar 

  • Paez-Espino D, Tamames J, de Lorenzo V, Canovas D (2009) Microbial responses to environmental arsenic. Biometals 22:117–130

    Article  CAS  Google Scholar 

  • Pepi M, Volterrani M, Renzi M, Marvasi M, Gasperini S, Franchi E, Focardi SE (2007) Arsenic-resistant bacteria isolated from contaminated sediments of the Orbetello Lagoon, Italy, and their characterization. J Appl Microbiol 103:2299–2308

    Article  CAS  Google Scholar 

  • Phung LT, Silver S, Trimble WL, Gilbert JA (2012) Draft genome of Halomonas species strain GFAJ-1 (ATCC BAA-2256). J Bacteriol 194:1835–1836

    Google Scholar 

  • Planer-Friedrich B, London J, McClesky RB, Nordstrom DK, Wallschläger D (2007) Thioarsenates in geothermal waters of yellowstone national park: determination, preservation, and geochemical importance. Env Sci Technol 41:5245–5251

    Article  CAS  Google Scholar 

  • Planer-Friedrich B, Suess E, Scheinost AC, Wallschläger D (2010) Arsenic speciation in sulfidic waters: reconciling contradictory spectroscopic and chromatographic evidence. Anal Chem 82:10228–10235

    Article  CAS  Google Scholar 

  • Platanias LC (2009) Biological responses to arsenic compounds. J Biol Chem 284:18583–18587

    Article  CAS  Google Scholar 

  • Qin J, Rosen BP, Zhang Y, Wang GJ, Franke S, Rensing C (2006) Arsenic detoxification and evolution of trimethylarsine gas by a microbial arsenite S-adenosylmethionine methyltransferase. Proc Natl Acad Sci USA 103:2075–2080

    Article  CAS  Google Scholar 

  • Raven KP, Jain A, Loeppert RH (1998) Arsenite and arsenate adsorption on ferrihydrite: kinetics, equilibrium, and adsorption envelopes. Environ Sci Technol 32:344–349

    Article  CAS  Google Scholar 

  • Reaves ML, Sinha S, Rabinowitz JD, Kruglyak L, Redfield RJ (2012) Absence of detectable arsenate in DNA from arsenate-grown GFAJ-1 Cells. Science 337(6093):470–473

    Article  CAS  Google Scholar 

  • Redfield RJ (2011) Comment on "A bacterium that can grow by using arsenic instead of phosphorus". Science 332(6034). doi:10.1126/science.1201482

  • Richey C, Chovanec P, Hoeft SE, Oremland RS, Basu P, Stolz JF (2009) Respiratory arsenate reductase as a bidirectional enzyme. Biochem Biophys Res Commun 382:298–302

    Article  CAS  Google Scholar 

  • Rosen BP (1999) Families of arsenic transporters. Trends Microbiol 7:207–212

    Article  CAS  Google Scholar 

  • Rosen BP (2002) Biochemistry of arsenic detoxification. FEBS Lett 529:86–92

    Article  CAS  Google Scholar 

  • Rosen BP, Liu ZJ (2009) Transport pathways for arsenic and selenium: a mini review. Environ Int 35:512–515

    Article  CAS  Google Scholar 

  • Rosen BP, Ajees AA, McDermott TR (2011) Life and death with arsenic life: an analysis of the recent report “A bacterium that can grow by using arsenic instead of phosphorus”. Bioessays 33:350–357

    Article  CAS  Google Scholar 

  • Ryan D, Colleran E (2002) Arsenical resistance in the IncHI2 plasmids. Plasmid 47:234–240

    Article  CAS  Google Scholar 

  • Saltikov CW, Wildman RA, Newman DK (2005) Expression dynamics of arsenic respiration and detoxification in Shewanella sp strain ANA-3. J Bacteriol 187:7390–7396

    Article  CAS  Google Scholar 

  • Sanders OI, Rensing C, Kuroda M, Rosen BP (1997) Antimonite is accumulated by the glycerol facilitator GlpFin Escherichia coli. J Bacteriol 179:3365–3367

    CAS  Google Scholar 

  • Santini JM, vanden Hoven RN (2004) Molybdenum-containing arsenite oxidase of the chemolithoautotrophic arsenite oxidizer NT-26. J Bacteriol 186:1614–1619

    Article  CAS  Google Scholar 

  • Santini JM, Sly LI, Schnagl RD, Macy JM (2000) A new chemolithoautotrophic arsenite-oxidizing bacterium isolated from a gold mine: phylogenetic, physiological, and preliminary biochemical studies. Appl Environ Microbiol 66:92–97

    Article  CAS  Google Scholar 

  • Sato T, Kobayashi Y (1998) The ars operon in the skin element of Bacillus subtilis confers resistance to arsenate and arsenite. J Bacteriol 180:1655–1661

    Google Scholar 

  • Sen Gupta B, Chatterjee S, Rott U, Kauffman H, Bandopadhyay A, DeGroot W, Nag NK, Carbonell-Barrachina AA, Mukherjee S (2009) A simple chemical free arsenic removal method for community water supply—a case study from West Bengal, India. Environ Pollut 157:3351–3353

    Article  CAS  Google Scholar 

  • Shakya S, Pradhan B, Smith L, Shrestha J, Tuladhar S (2012) Isolation and characterization of aerobic culturable arsenic-resistant bacteria from surfacewater and groundwater of Rautahat District, Nepal. J Environ Manage 95:S250–S255

    Article  CAS  Google Scholar 

  • Sherwood Lollar B (2005) Environmental geochemistry. Elsevier, Amsterdam

    Google Scholar 

  • Shi J, Vlamis-Gardikas V, Aslund F, Holmgren A, Rosen BP (1999) Reactivity of glutaredoxins 1, 2, and 3 from Escherichia coli shows that glutaredoxin 2 is the primary hydrogen donor to ArsC-catalyzed arsenate reduction. J Biol Chem 274:36039–36042

    Article  CAS  Google Scholar 

  • Siegfried K, Endes C, Bhuiyan AFMK, Kuppardt A, Mattusch J, van der Meer JR, Chatzinotas A, Harms H (2012) Field testing of arsenic in groundwater samples of Bangladesh using a test kit based on lyophilized bioreporter bacteria. Environ Sci Technol 46:3281–3287

    Article  CAS  Google Scholar 

  • Sierra-Alvarez R, Yenal U, Field JA, Kopplin M, Gandolfi AJ, Garbarino JR (2006) Anaerobic biotransformation of organoarsenical pesticides monomethylarsonic acid and dimethylarsinic acid. J Agric Food Chem 54:3959–3966

    Article  CAS  Google Scholar 

  • Silver S (1998) Genes for all metals—a bacterial view of the periodic table—the 1996 Thom award lecture. J Ind Microbiol Biot 20:1–12

    Article  CAS  Google Scholar 

  • Silver S, Phung LT (2005) Genes and enzymes involved in bacterial oxidation and reduction of inorganic arsenic. Appl Environ Microbiol 71:599–608

    Article  CAS  Google Scholar 

  • Simmons SL, DiBartolo G, Denef VJ, Goltsman DSA, Thelen MP, Banfield JF (2008) Population genomic analysis of strain variation in Leptospirillum group II bacteria involved in acid mine drainage formation. PLoS Biol 6:1427–1442

    Article  CAS  Google Scholar 

  • Smedley PL, Kinniburgh DG (2002) A review of the source, behaviour and distribution of arsenic in natural waters. Appl Geochem 17:517–568

    Article  CAS  Google Scholar 

  • Stocker J, Balluch D, Gsell M, Harms H, Feliciano J, Daunert S, Malik KA, Van der Meer JR (2003) Development of a set of simple bacterial biosensors for quantitative and rapid measurements of arsenite and arsenate in potable water. Environ Sci Technol 37:4743–4750

    Article  CAS  Google Scholar 

  • Stolz JF, Oremland RS (1999) Bacterial respiration of arsenic and selenium. FEMS Microbiol Rev 23:615–627

    Article  CAS  Google Scholar 

  • Stolz JE, Basu P, Santini JM, Oremland RS (2006) Arsenic and selenium in microbial metabolism. Annu Rev Microbiol 60:107–130

    Article  CAS  Google Scholar 

  • Styblo M, Del Razo LM, Vega L, Germolec DR, LeCluyse EL, Hamilton GA, Reed W, Wang C, Cullen WR, Thomas DJ (2000) Comparative toxicity of trivalent and pentavalent inorganic and methylated arsenicals in rat and human cells. Arch Toxicol 74:289–299

    Article  CAS  Google Scholar 

  • Sun WJ, Sierra-Alvarez R, Field JA (2011) Long term performance of an arsenite-oxidizing-chlorate-reducing microbial consortium in an upflow anaerobic sludge bed (UASB) bioreactor. Bioresour Technol 102:5010–5016

    Article  CAS  Google Scholar 

  • Trang PTK, Berg M, Viet PH, Van Mui N, Van Der Meer JR (2005) Bacterial bioassay for rapid and accurate analysis of arsenic in highly variable groundwater samples. Environ Sci Technol 39:7625–7630

    Article  CAS  Google Scholar 

  • Tsai SL, Singh S, Chen W (2009) Arsenic metabolism by microbes in nature and the impact on arsenic remediation. Curr Opin Biotech 20:659–667

    Article  CAS  Google Scholar 

  • Tuffin IM, Hector SB, Deane SM, Rawlings DE (2006) Resistance determinants of a highly arsenic-resistant strain of Leptospirillum ferriphilum isolated from a commercial biooxidation tank. Appl Environ Microbiol 72:2247–2253

    Article  CAS  Google Scholar 

  • Turner AW (1949) Bacterial oxidation of arsenite. Nature 164(4158):76–77

    Article  CAS  Google Scholar 

  • van Halem D, Olivero S, de Vet WWJM, Verberk JQJC, Amy GL, van Dijk JC (2010) Subsurface iron and arsenic removal for shallow tube well drinking water supply in rural Bangladesh. Water Res 44:5761–5769

    Article  CAS  Google Scholar 

  • vanden Hoven RN, Santini JM (2004) Arsenite oxidation by the heterotroph Hydrogenophaga sp str. NT-14: the arsenite oxidase and its physiological electron acceptor. Biochim Biophys Acta Bioenerg 1656:148–155

    Article  CAS  Google Scholar 

  • Vithanage M, Dabrowska BB, Mukherjee AB, Sandhi A, Bhattacharya P (2012) Arsenic uptake by plants and possible phytoremediation applications: a brief overview. Environ Chem Lett 10:217–224

    Article  CAS  Google Scholar 

  • Wang LP, Jeon BW, Sahin O, Zhang QJ (2009) Identification of an arsenic resistance and arsenic-sensing system in Campylobacter jejuni. Appl Environ Microbiol 75:5064–5073

    Article  CAS  Google Scholar 

  • Wang Q, Xiong D, Zhao P, Yu X, Tu B, Wang G (2011) Effect of applying an arsenic-resistant and plant growth-promoting rhizobacterium to enhance soil arsenic phytoremediation by Populus deltoides LH05-17. J Appl Microbiol 111:1065–1074

    Article  CAS  Google Scholar 

  • Waychunas GA, Rea BA, Fuller CC, Davis JA (1993) Surface-chemistry of ferrihydrite. Part 1. EXAFS studies of the geometry of coprecipitated and adsorbed arsenate. Geochim Cosmochim Acta 57:2251–2269

    Article  CAS  Google Scholar 

  • Weeger W, Lievremont D, Perret M, Lagarde F, Hubert JC, Leroy M, Lett MC (1999) Oxidation of arsenite to arsenate by a bacterium isolated from an aquatic environment. Biometals 12:141–149

    Article  CAS  Google Scholar 

  • Weiss S, Carapito C, Cleiss J, Koechler S, Turlin E, Coppee JY, Heymann M, Kugler V, Stauffert M, Cruveiller S, Medigue C, Van Dorsselaer A, Bertin PN, Arsene-Ploetze F (2009) Enhanced structural and functional genome elucidation of the arsenite-oxidizing strain Herminiimonas arsenicoxydans by proteomics data. Biochimie 91:192–203

    Article  CAS  Google Scholar 

  • Welch AH, Westjohn DB, Helsel DR, Wanty RB (2000) Arsenic in ground water of the United States: occurrence and geochemistry. Ground Water 38:589–604

    Article  CAS  Google Scholar 

  • Westheimer FH (1987) Why nature chose phosphates. Science 235(4793):1173–1178

    Article  CAS  Google Scholar 

  • WHO (1996) Guidelines for drinking-water quality, 2nd edition, Vol 2. Health criteria and other supporting information. World Health Organization, Geneva

    Google Scholar 

  • Wilkins MJ, VerBerkmoes NC, Williams KH, Callister SJ, Mouser PJ, Elifantz H, N’Guessan AL, Thomas BC, Nicora CD, Shah MB, Abraham P, Lipton MS, Lovley DR, Hettich RL, Long PE, Banfield JF (2009) Proteogenomic monitoring of Geobacter physiology during stimulated uranium bioremediation. Appl Environ Microbiol 75:6591–6599

    Article  CAS  Google Scholar 

  • Willsky GR, Malamy MH (1980a) Characterization of 2 genetically separable inorganic-phosphate transport-systems in Escherichia coli. J Bacteriol 144:356–365

    CAS  Google Scholar 

  • Willsky GR, Malamy MH (1980b) Effect of arsenate on inorganic-phosphate transport in Escherichia coli. J Bacteriol 144:366–374

    CAS  Google Scholar 

  • Wolfe-Simon F, Blum JS, Kulp TR, Gordon GW, Hoeft SE, Pett-Ridge J, Stolz JF, Webb SM, Weber PK, Davies PCW, Anbar AD, Oremland RS (2011) A bacterium that can grow by using arsenic instead of phosphorus. Science 332(6034):1163–1166

    Article  CAS  Google Scholar 

  • Wu J, Rosen BP (1991) The ArsR protein is a trans-acting regulatory protein. Mol Microbiol 5:1331–1336

    Article  CAS  Google Scholar 

  • Xu C, Zhou TQ, Kuroda M, Rosen BP (1998) Metalloid resistance mechanisms in prokaryotes. J Biochem-Tokyo 123:16–23

    Article  CAS  Google Scholar 

  • Yang H-C, Cheng J, Finan TM, Rosen BP, Bhattarcharjee H (2005) Novel pathway for arsenic detoxification in the legume symbiont Sinorhizobium meliloti. J Bacteriol 187:6991–6997

    Article  CAS  Google Scholar 

  • Yang JB, Rawat S, Stemmler TL, Rosen BP (2010) Arsenic binding and transfer by the ArsD As(III) metallochaperone. Biochemistry-US 49:3658–3666

    Article  CAS  Google Scholar 

  • Ye J, Rensing C, Rosen BP, Zhu Y-G (2012) Arsenic biomethylation by photosynthetic organisms. Trends Plant Sci 17:155–162

    Article  CAS  Google Scholar 

  • Yoshinaga M, Cai Y, Rosen BP (2011) Demethylation of methylarsonic acid by a microbial community. Environ Microbiol 13:1205–1215

    Article  CAS  Google Scholar 

  • Zargar K, Hoeft S, Oremland R, Saltikov CW (2010) Identification of a novel arsenite oxidase gene, arxA, in the haloalkaliphilic, arsenite-oxidizing bacterium Alkalilimnicola ehrlichii strain MLHE-1. J Bacteriol 192:3755–3762

    Article  CAS  Google Scholar 

  • Zargar K, Conrad A, Bernick DL, Lowe TM, Stolc V, Hoeft S, Oremland RS, Stolz J, Saltikov CW (2012) ArxA, a new clade of arsenite oxidase within the DMSO reductase family of molybdenum oxidoreductases. Environ Microbiol 14:1635–1645

    Article  CAS  Google Scholar 

  • Zegers I, Martins JC, Willem R, Wyns L, Messens J (2001) Arsenate reductase from S. aureus plasmid pI258 is a phosphatase drafted for redox duty. Nat Struct Biol 8:843–847

    Article  CAS  Google Scholar 

  • Zhao FJ, McGrath SP, Meharg AA (2010) Arsenic as a food chain contaminant: mechanisms of plant uptake and metabolism and mitigation strategies. Annu Rev Plant Biol 61:535–559

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was partially supported by the European Commission within its Seventh Framework Program Project BACSIN (Contract No. 211684) and by the EC2CO program (INEE, CNRS), the RARE (ANR 07-BLANC-0118) and the MULTIPOLSITE (ANR-2008-CESA-010) projects (Agence Nationale de la Recherche, France). Florence Arsène-Ploetze was supported by the CNRS (“mise en délégation pour activité de recherche au CNRS”). This work contributed to the CITE Research Programme of the Helmholtz Centre for Environmental Research.

Author information

Author notes

  1. Martin C. Kruger

    Present address: Department of Environmental Microbiology, Helmholtz Centre for Environmental Research-UFZ, Permoserstr. 15, 04318, Leipzig, Germany

Authors and Affiliations

  1. Department of Environmental Biotechnology, Helmholtz Centre for Environmental Research-UFZ, Permoserstr. 15, 04318, Leipzig, Germany

    Martin C. Kruger & Hermann J. Heipieper

  2. Laboratoire de Génétique Moléculaire, Génomique et Microbiologie, Université de Strasbourg, CNRS-UMR7156, 28, rue Goethe, 67083, Strasbourg, France

    Philippe N. Bertin & Florence Arsène-Ploetze

Authors
  1. Martin C. Kruger
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Philippe N. Bertin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hermann J. Heipieper
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Florence Arsène-Ploetze
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hermann J. Heipieper.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kruger, M.C., Bertin, P.N., Heipieper, H.J. et al. Bacterial metabolism of environmental arsenic—mechanisms and biotechnological applications. Appl Microbiol Biotechnol 97, 3827–3841 (2013). https://doi.org/10.1007/s00253-013-4838-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-013-4838-5

Keywords

Search

Navigation